Endoplasmic reticulum proteostasis contributes to shape plant immunity: Perspectives from plant and pathogen sides

The endoplasmic reticulum (ER) is the gate to the secretory pathway for at least one third of the newly synthesized proteins. Its proper function is essential for keeping cellular homeostasis during plant development and responses to environmental cues. Plants have evolved a wide set of cellular and molecular systems that allow to maintain a delicate balance between protein synthesis, folding, and degradation. Among these, ER quality control (ER-QC) plays key roles. However, biotic and abiotic stresses can disrupt this balance, leading to protein homeostasis disturbance and ER stress. This can lead to programmed cell death under acute conditions. To cope with this, plant cells activate the unfolded protein response (UPR) to restore ER and cellular homeostasis. Increasing evidence shows that UPR signaling has a significant impact on plant immunity. This supports the concept of ER stress-mediated immunity (ERSI), in which the UPR drives plant immunity. In contrast, pathogen effectors can manipulate host protein homeostasis to facilitate infection. In addition, recent results reveal that the ER proteostasis of plant-interacting pathogens is involved in pathogenicity. In this review, we discuss the latest findings on ER protein homeostasis, with a particular focus on its interplay with plant immunity. We also explore how pathogens manipulate the ER proteostasis of the host cell and propose a model where both partners exploit each other's ER proteostasis for their own advantage. • The endoplasmic reticulum quality control and the unfolded protein response play a pivotal role in plant immunity • Maintaining endoplasmic reticulum proteostasis is crucial for fungal pathogenicity • Pathogens effectors target endoplasmic reticulum proteostasis during the infection process • Plant triggers endoplasmic reticulum stress in pathogens through phytoalexins • Characterization of endoplasmic reticulum proteostasis involvement in plant-pathogen interactions opens prospects for new protection strategies